Target and non-target effects of insecticide use during ornamental milkweed production.

There are widespread public efforts to conserve wildlife in urbanized landscapes via the installation of nursery-grown plants that support Lepidoptera taxa. Insecticides are commonly used during nursery production to suppress key plant pests, and many products have extended periods of toxicity and affect a wide range of herbivore taxa. While there are plentiful toxicological data on bee species, predominantly the Western honey bee (Apis mellifera L.), little is known about how insecticides affect nonpest lepidopterans. Lepidoptera has different modes of exposure (e.g., leaf-feeding) and differences in susceptibility to insecticide target sites compared to bees. Consequently, many products compatible with bee conservation pose an uncertain risk to nonpest lepidopterans and thus may represent an under-recognized conflict with conservation efforts. Using the monarch butterfly (Danaus plexippus, L.), tropical milkweed (Asclepias curassavica, L.), and oleander aphid (Aphis nerii, Fonscolombe, 1841) system, we conducted leaf and whole-plant feeding assays to evaluate effects of acute and chronic monarch exposure to industry standard and alternative reduced-risk insecticides used during nursery production. We also evaluated the efficacy of these insecticides against their target pest, the oleander aphid. Our results indicate that insecticides used to control pests on ornamental milkweed can cause monarch larval mortality up to 4 wk after treatment application. Furthermore, the duration of aphid suppression is often shorter than the duration of adverse effects on monarchs. This study demonstrates a conflict between insect pest management and Lepidoptera conservation during ornamental plant production and has implications for the conservation value of ornamentals after retail sale.

Aphid infestations reduce monarch butterfly colonization, herbivory, and growth on ornamental milkweed.

Anthropogenic disturbance is driving global biodiversity loss, including the monarch butterfly (Danaus plexippus), a dietary specialist of milkweed. In response, ornamental milkweed plantings are increasingly common in urbanized landscapes, and recent evidence indicates they have conservation value for monarch butterflies. Unfortunately, sap-feeding insect herbivores, including the oleander aphid (Aphis nerii), frequently reach high densities on plants in nursery settings and urbanized landscapes. Aphid-infested milkweed may inhibit monarch conservation efforts by reducing host plant quality and inducing plant defenses. To test this, we evaluated the effects of oleander aphid infestation on monarch oviposition, larval performance, and plant traits using tropical milkweed (Asclepias curassavica), the most common commercially available milkweed species in the southern U.S. We quantified monarch oviposition preference, larval herbivory, larval weight, and plant characteristics on aphid-free and aphid-infested milkweed. Monarch butterflies deposited three times more eggs on aphid-free versus aphid-infested milkweed. Similarly, larvae fed aphid-free milkweed consumed and weighed twice as much as larvae fed aphid-infested milkweed. Aphid-free milkweed had higher total dry leaf biomass and nitrogen content than aphid-infested milkweed. Our results indicate that oleander aphid infestations can have indirect negative impacts on urban monarch conservation efforts and highlight the need for effective Lepidoptera-friendly integrated pest management tactics for ornamental plants.

Mixed-Species Gardens Increase Monarch Oviposition without Increasing Top-Down Predation.

Monarch butterfly populations have declined by over 80% in the last 20 years. Conservation efforts focus on the creation of milkweed habitats to mitigate this decline. Previous research has found monarchs lay more eggs per milkweed stem in urban gardens than natural habitats and recent work identified specific garden designs that make urban gardens more attractive to monarchs. Increasing plant diversity can reduce specialist insect herbivore colonization via bottom-up (e.g., plant) and top-down (e.g., predation) regulatory factors. Although this is beneficial for pest management efforts, it contradicts conservation efforts. In this study, we explored if adding multiple flowering species to garden-sized milkweed plantings affected monarch oviposition or top-down regulation of larvae. We compared monarch egg abundance, natural enemy abundance and richness, and biological control of monarch larvae in milkweed monocultures and milkweed mixed with four additional wildflower species. We found that monarchs laid 22% more eggs on sentinel milkweed plants in mixed-species plots with no effect of plant diversity on monarch survival. We also found higher natural enemy richness, wasp, and predatory bug abundance in the mixed-species plots and this did not translate to higher biological control rates. Our results provide more evidence that plant selection and habitat design are important for monarch conservation.

Native and Edible Ornamental Plant Congeners Enhance Ecosystem Services Through Key Pest Avoidance and Multifunctionality in Residential Landscapes.

Tea scale, Fiorinia theae Green (Hemiptera: Diaspididae), has long been one of the most important pests of Ilex and Camellia plants, particularly in the southeastern United States. This exotic armored scale insect reduces host plant health and function, and often requires insecticide use, which poses risks to nontarget organisms. While the use of Ilex (Aquifoliales: Aquifoliaceae) and Camellia (Ericales: Theaceae) spp. as landscape ornamentals for aesthetic function is firmly established, we have a poor understanding of species-level susceptibility to F. theae. Additionally, two species, Ilex vomitoria Ait. and Camellia sinensis (L.) O. Kuntze are emerging tisane- and tea-producing commodities in the region, respectively. We propose that these consumable plants may be well-suited alternatives to their traditionally used ornamental congeners in residential landscapes where they may provide enhanced ecosystem services. However, the potential impact of key pests, like F. theae, on these species should be evaluated to anticipate pest pressure that may undermine or offset benefits. In this study, we examine six species within the known host range of tea scale, comparing nonnative I. cornuta Lindl. 'Dwarf Burford,' C. japonica L., C. sasanqua Thunb., and C. sinensis, along with native I. opaca Ait. and I. vomitoria. We found that plant species show a wide range of susceptibility to F. theae and associated damage, with the two native Ilex species and tea-producing C. sinensis displaying the least susceptibility. By reducing the impact of a key pest and considering other ecosystem service traits, these results may help guide more sustainable plant selection decisions where the goal is to integrate native and edible plants into residential landscapes.

Turfgrass Cultivar Diversity Provides Associational Resistance in the Absence of Pest Resistant Cultivars.

Turfgrasses are ubiquitous in urban landscapes and can provide numerous ecosystem services. However, most warm season turfgrasses are produced, planted, and maintained as cultivar monocultures, which may predispose them to herbivore attack and reduce the services lawns provide. Though rarely done, host plant resistance can be used as a strategy to reduce herbivory and preserve beneficial services. Increasing turfgrass cultivar diversity may provide similar or greater benefits through associational resistance, whereas conserving desirable maintenance and aesthetic traits. However, no studies have examined this in warm season turfgrasses. To address this, we evaluated host plant resistance to fall armyworm (Spodoptera frugiperda [J.E. Smith] [Lepidoptera: Noctuidae]) in commercially available cultivars of St. Augustinegrass (Stenotaphrum secundatum [(Walt.) Kuntz] [Lepidoptera: Noctuidae]) and then investigated if the resistance or susceptibility of St. secundatum cultivars carried over in mixed cultivar plantings. Through a no-choice experiment and a limited-choice experiment, we detected no host plant resistance in monocultures of St. secundatum cultivars. However, we did find that as cultivar diversity increased, female Sp. frugiperda larval weight and herbivory decreased. Additionally, choice tests indicated that larvae prefer less diverse stands of St. secundatum cultivars. Interestingly, our results suggest that in the absence of host plant resistance, warm season turfgrass cultivar diversity may reduce herbivore pest fitness and damage. These results demonstrate that warm season turfgrass cultivar diversity may be a viable integrated pest management tool that warrants further investigation.

Urban plants and climate drive unique arthropod interactions with unpredictable consequences.

Urban areas, a rapidly expanding land cover type, are composed of a mix of impervious surfaces, ornamental plants, and remnant habitat, which alters abiotic conditions and affects arthropod community assemblages and trophic interactions. Importantly, these effects often reduce arthropod diversity and may increase, reduce, or not change individual species or trophic interactions, which affects human and environmental health. Despite the pace of urbanization, drivers and consequences of change in urban arthropod communities remains poorly understood. Here, we review recent findings that shed light on the effects of urbanization on plants and abiotic conditions that drive arthropod community composition and trophic interactions, with discussion of how these effects conflict with human values and can be mitigated for future urbanization.

Warming and drought combine to increase pest insect fitness on urban trees.

Urban habitats are characterized by impervious surfaces, which increase temperatures and reduce water availability to plants. The effects of these conditions on herbivorous insects are not well understood, but may provide insight into future conditions. Three primary hypotheses have been proposed to explain why multiple herbivorous arthropods are more abundant and damaging in cities, and support has been found for each. First, less complex vegetation may reduce biological control of pests. Second, plant stress can increase plant quality for pests. And third, urban warming can directly increase pest fitness and abundance. These hypotheses are not mutually exclusive, and the effects of temperature and plant stress are particularly related. Thus, we test the hypothesis that urban warming and drought stress combine to increase the fitness and abundance of the scale insect, Melanaspis tenebricosa, an urban tree pest that is more abundant in urban than rural areas of the southeastern U.S. We did this by manipulating drought stress across an existing mosaic of urban warming. We found support for the additive effect of temperature and drought stress such that female embryo production and body size increased with temperature and was greater on drought-stressed than watered trees. This study provides further evidence that drivers of pest insect outbreaks act in concert, rather than independently, and calls for more research that manipulates multiple abiotic factors related to urbanization and climate change to predict their effects on ecological interactions. As cities expand and the climate changes, warmer temperatures and drought conditions may become more widespread in the native range of this pest. These changes have direct physiological benefits for M. tenebricosa, and potentially other pests, that may increase their fitness and abundance in urban and natural forests.

Do cities simulate climate change? A comparison of herbivore response to urban and global warming.

Cities experience elevated temperature, CO2 , and nitrogen deposition decades ahead of the global average, such that biological response to urbanization may predict response to future climate change. This hypothesis remains untested due to a lack of complementary urban and long-term observations. Here, we examine the response of an herbivore, the scale insect Melanaspis tenebricosa, to temperature in the context of an urban heat island, a series of historical temperature fluctuations, and recent climate warming. We survey M. tenebricosa on 55 urban street trees in Raleigh, NC, 342 herbarium specimens collected in the rural southeastern United States from 1895 to 2011, and at 20 rural forest sites represented by both modern (2013) and historical samples. We relate scale insect abundance to August temperatures and find that M. tenebricosa is most common in the hottest parts of the city, on historical specimens collected during warm time periods, and in present-day rural forests compared to the same sites when they were cooler. Scale insects reached their highest densities in the city, but abundance peaked at similar temperatures in urban and historical datasets and tracked temperature on a decadal scale. Although urban habitats are highly modified, species response to a key abiotic factor, temperature, was consistent across urban and rural-forest ecosystems. Cities may be an appropriate but underused system for developing and testing hypotheses about biological effects of climate change. Future work should test the applicability of this model to other groups of organisms.

The effects of urban warming on herbivore abundance and street tree condition.

Trees are essential to urban habitats because they provide services that benefit the environment and improve human health. Unfortunately, urban trees often have more herbivorous insect pests than rural trees but the mechanisms and consequences of these infestations are not well documented. Here, we examine how temperature affects the abundance of a scale insect, Melanaspis tenebricosa (Comstock) (Hemiptera: Diaspididae), on one of the most commonly planted street trees in the eastern U.S. Next, we examine how both pest abundance and temperature are associated with water stress, growth, and condition of 26 urban street trees. Although trees in the warmest urban sites grew the most, they were more water stressed and in worse condition than trees in cooler sites. Our analyses indicate that visible declines in tree condition were best explained by scale-insect infestation rather than temperature. To test the broader relevance of these results, we extend our analysis to a database of more than 2700 Raleigh, US street trees. Plotting these trees on a Landsat thermal image of Raleigh, we found that warmer sites had over 70% more trees in poor condition than those in cooler sites. Our results support previous studies linking warmer urban habitats to greater pest abundance and extend this association to show its effect on street tree condition. Our results suggest that street tree condition and ecosystem services may decline as urban expansion and global warming exacerbate the urban heat island effect. Although our non-probability sampling method limits our scope of inference, our results present a gloomy outlook for urban forests and emphasize the need for management tools. Existing urban tree inventories and thermal maps could be used to identify species that would be most suitable for urban conditions.

Urban warming trumps natural enemy regulation of herbivorous pests.

Trees provide ecosystem services that counter negative effects of urban habitats on human and environmental health. Unfortunately, herbivorous arthropod pests are often more abundant on urban than rural trees, reducing tree growth, survival, and ecosystem services. Previous research where vegetation complexity was reduced has attributed elevated urban pest abundance to decreased regulation by natural enemies. However, reducing vegetation complexity, particularly the density of overstory trees, also makes cities hotter than natural habitats. We ask how urban habitat characteristics influence an abiotic factor, temperature, and a biotic factor, natural enemy abundance, in regulating the abundance of an urban forest pest, the gloomy scale, (Melanaspis tenebricosa). We used a map of surface temperature to select red maple trees (Acer rubrum) at warmer and cooler sites in Raleigh, North Carolina, USA. We quantified habitat complexity by measuring impervious surface cover, local vegetation structural complexity, and landscape scale vegetation cover around each tree. Using path analysis, we determined that impervious surface (the most important habitat variable) increased scale insect abundance by increasing tree canopy temperature, rather than by reducing natural enemy abundance or percent parasitism. As a mechanism for this response, we found that increasing temperature significantly increases scale insect fecundity and contributes to greater population increase. Specifically, adult female M. tenebricosa egg sets increased by approximately 14 eggs for every 1°C increase in temperature. Climate change models predict that the global climate will increase by 2­3°C in the next 50­100 years, which we found would increase scale insect abundance by three orders of magnitude. This result supports predictions that urban and natural forests will face greater herbivory in the future, and suggests that a primary cause could be direct, positive effects of warming on herbivore fitness rather than altered trophic interactions.